The rhizosphere and cropping system, but not arbuscular mycorrhizae, affect ammonia oxidizing archaea and bacteria abundances in two agricultural soils

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Highlights

  • AMF alter inorganic N pools, but not AOB or AOA abundances in N-rich soils.

  • AOA abundance was elevated in the maize rhizosphere compared to bulk soil.

  • AOB were more abundant in soil with increased inorganic N fertilization.

  • Differing ecological niches exist for AOA and AOB in agricultural soils.

Abstract

Arbuscular mycorrhizal fungi (AMF) form symbioses with roots that can enhance plant nutrition. While AMF have been shown to have a role in soil nitrogen (N) cycling, it is unclear whether AMF affect N cycling microbes such as ammonia-oxidizing bacteria (AOB) and archaea (AOA), which convert ammonium into nitrite in the first step of nitrification. In this study, we examined the effects of AMF on AOA and AOB abundances within the corn rhizosphere and bulk soil of conventional (corn-soybean rotation with inorganic fertilizer) and diversified (corn-soybean-oats/alfalfa-oats rotation with composted manure) systems. We hypothesized that AMF would decrease AOA and AOB abundances in a cropping-system dependent manner, possibly due to competition for ammonium. We grew corn deficient or proficient in AMF symbiosis in microcosms for 10 weeks. At the end of the experiment, both soils planted with the AMF-proficient corn genotype had higher ammonium and lower nitrate pool sizes compared to the same soils planted with the AMF-deficient corn genotype. Likewise, total plant N was higher in the AMF-proficient genotype compared to the AMF-deficient genotype. Despite changes in soil inorganic N pool sizes, AOA and AOB abundances were unaffected by plant AMF-proficiency. Instead, AOA abundance was greater in the rhizosphere than in the bulk soil regardless of cropping system, and AOB abundance was greater in the conventional than the diversified cropping system soil regardless of proximity to the root. These data indicate that 1) AMF did not affect AOA or AOB abundance in these N-rich soils but other factors such as root proximity and inorganic fertilization did and 2) AOA and AOB have differing ecological niches within rhizosphere and bulk soil that should be considered when managing for nitrogen losses.

Introduction

Ammonia oxidizers (AO), comprised of bacteria (AOB) and archaea (AOA), play an important role in the nitrogen (N) cycle. AO mediate the first step of nitrification, the process which converts ammonium (NH4+) to nitrate (NO3). Nitrification has become a key issue in agricultural soils where ammonium and urea fertilizers are often applied in excess of, or in asynchronous timing to, what crops are able to use. The NO3 that results is easily leached into waterways where it can cause hypoxia and ecological damage. An extreme example of this is the “dead-zone” of the Gulf of Mexico that is largely caused by leachates from midwestern agriculture (Burkart and James, 1999; Carpenter et al., 1998; Di and Cameron, 2002). It is vital that we understand the fate of N in our arable soils to improve nitrogen use efficiency.

Due to the pivotal role that AO play in nitrification, it is important that we understand the factors that shape their growth and metabolic activities. Many studies have shown that abiotic factors such as pH, temperature, soil depth, and fertilization history influence the abundance and activity of AO (Di et al., 2010; Nicol et al., 2008; Ouyang et al., 2017; Tourna et al., 2008; Wessén et al., 2010a). Yet, we know little about how biotic factors may influence AO abundance, diversity, or metabolism in soil. For example, the rhizosphere effect can increase AO abundance relative to bulk (root-free) soil (Ai et al., 2013; Dias et al., 2012; Hussain et al., 2011). Additionally, gross nitrification rates are elevated in the Avena barbata rhizosphere and dependent on the location along the root (Herman et al., 2006). The most likely mechanisms that could cause changes in AO growth in the root zone include rhizodeposition and decomposition of dead root material that may cause changes in N mineralization and uptake in the surrounding soil (Ai et al., 2013; Dias et al., 2012; Frank and Groffman, 2009; Hussain et al., 2011). Biotic interactions may play an important, though underexplored, role in determining AO abundance and activity in soils.

There is also limited knowledge about biotic interactions between AO and other microorganisms. Of particular interest are the arbuscular mycorrhizal fungi (AMF) that form symbioses with plant roots. AMF hyphae acquire nutrients for the plant in exchange for photosynthetic carbon, acting as an extension of the root system. It is becoming evident that AMF play a more important role in the soil N cycling than previously thought (Veresoglou et al., 2012) and could be potential competitors with AO for NH4+. For instance, increased uptake of inorganic N by AMF inoculated plants can reduce NH4+ and NO3 leaching from soils (Asghari and Cavagnaro, 2011; Bender et al., 2014; Cavagnaro et al., 2015; Corkidi et al., 2011; Köhl and van der Heijden, 2016). Additionally, this nutrient displacement can have effects on the associated microbial community; inorganic nitrogen absorption by AMF was found to alter the microbial community of decomposing litter (Nuccio et al., 2013). Because AO are relatively poor competitors for NH4+ compared to heterotrophic microbes (Verhagen and Laanbroek, 1991; Verhagen et al., 1995) and AMF are thought to prefer NH4+ to NO3 when transferring N to plant hosts (Govindarajulu et al., 2005; Tanaka and Yano, 2005), AMF may be able to outcompete AO for the same NH4+ pool and therefore have an inhibitory effect on AO growth or activity.

Despite previous efforts, inconsistent findings have made it difficult to develop a robust model of potential interactions between AMF and AO; AMF have been found to increase, decrease, or have little impact on AO abundance or metabolic activity (Amora-Lazcano et al., 1998; Cavagnaro et al., 2007; Chen et al., 2013; Veresoglou et al., 2011). In this study, our goal was to assess whether there are common or cropping system specific interactions between AMF and AO. We hypothesized that AMF colonization of corn roots would decrease soil AO abundance and that this effect would be larger in a diversified (four-year rotation, manure amendments) compared to a conventional (two-year rotation, inorganic fertilization) cropping system soil due to lower NH4+ availability and increased AMF community function. Our approach was to compare an AMF-deficient genotype of corn (a loss-of-function allele of the corn homolog of the dmi1 gene) to an AMF-proficient wild-type progenitor (Ané et al., 2004). This approach permitted minimal disturbance of the native microbial communities because soil sterilization was not necessary to establish an AMF-free treatment. Furthermore, with this method we could take advantage of the native AMF communities as shaped by soil management rather than inoculating the soils with AMF cultures. In this study, these AMF-proficient and deficient corn genotypes were grown in rhizotrons filled with soils from conventional or diversified cropping system plots. The abundances of AOA and AOB amoA genes (which transcribe the enzyme responsible for the rate-limiting step of nitrification) were measured by quantitative PCR (qPCR) to measure AO abundance in rhizosphere and bulk soils.

Section snippets

Field site and soil collection

We collected soils from the Iowa State University Marsden Long-Term Cropping System Experiment located in Boone County, IA (42°01′ N; 93°47′ W; 333 m above sea level). The Marsden site experiment examines three cropping systems differing in rotation complexity and fertilizer sources (Davis et al., 2012). In this study, we examined a conventional system comprised of a two-year rotation (soybean, corn) with inorganic N fertilizer and herbicide application comparable to surrounding commercial

Mycorrhizal abundance, colonization, and plant nutrition

Abundance of the 16:1ω5 fatty acid was significantly reduced in soils with the AMF-deficient compared to the AMF-proficient corn (Fig. 1). However, there were no significant impacts of cropping system, rhizosphere effect, or any interactions on 16:1ω5 fatty acid abundance (Fig. 1). Likewise, root colonization was significantly greater in AMF-proficient plant roots compared to AMF-deficient plant roots (2-way ANOVA, P < 0.001, Table 1) but did not differ significantly between cropping systems

Discussion

Understanding the ecology of AO and the factors that influence their growth is important due to the environmental damage caused by nitrification in agricultural soils. In this study, we used AMF-proficient and deficient corn genotypes to investigate biotic interactions between AMF and AO in soils from two agricultural systems with contrasting management. We hypothesized that AMF would decrease AO abundance in an agricultural system-specific manner, and we thought this because AMF may compete

Conclusions

In two contrasting agricultural soils, conventional and diversified, AMF did not affect AOA or AOB abundance. Instead, the rhizosphere increased AOA abundance compared to the bulk soil, possibly via growth on root exudates, while the conventional cropping system soil increased AOB abundance compared to diversified system soil, likely due to increased inorganic N application. Rather than reduce NH4+ availability in the soil as hypothesized, soils planted with AMF-proficient corn corresponded

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

Funding: This work was supported by the United States Department of Agriculture [grant number 2014-67019-21628] and University of Minnesota internal funding. This material is based upon work supported by Larry Halverson while serving at the U.S. NSF. Any opinion, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the U.S. NSF. We thank Guillaume Bay, Gregory Watson, and Alyssa Nease for their assistance

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